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Semin Plast Surg 2007; 21(4): 242-249
DOI: 10.1055/s-2007-991194
© Thieme Medical Publishers

Experience with Nerve Allograft Transplantation

Ida K. Fox1 , Susan E. Mackinnon1
  • 1Division of Plastic Surgery, Washington University School of Medicine, Saint Louis, Missouri
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Publication History

Publication Date:
27 November 2007 (online)

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ABSTRACT

Nerve allograft transplantation should be used for the repair of devastating peripheral nerve injuries that cannot be reconstructed through traditional means such as autologous nerve grafting or nerve transfer procedures. The risks of required systemic immunosuppression, although only temporary for nerve allograft recipients, preclude widespread use of this treatment modality. Translational research has led to several advancements in this field including the use of preoperative allograft cold preservation in University of Wisconsin organ preservation solution and inclusion of tacrolimus as part of the immunosuppressive regimen. Investigation of how to further diminish nerve allograft immunogenicity, speed neuroregeneration by use of agents such as tacrolimus, and promote preferential motor regeneration will further advance this field with the goal of restoring optimal function while minimizing patient morbidity.

KEYWORDS

Peripheral nerve - allograft - transplantation

REFERENCES

  • 1 Brenner M J, Tung T H, Jensen J N, Mackinnon S E. The spectrum of complications of immunosuppression: is the time right for hand transplantation?.  J Bone Joint Surg Am. 2002;  84A 1861-1870
    PubMedGoogle Scholar
  • 2 Henry M L. Cyclosporine and tacrolimus (FK506): a comparison of efficacy and safety profiles.  Clin Transplant. 1999;  13 209-220
    CrossrefPubMedGoogle Scholar
  • 3 Hooks M A. Tacrolimus, a new immunosuppressant-a review of the literature.  Ann Pharmacother. 1994;  28 501-511
    PubMedGoogle Scholar
  • 4 Lanzetta M, Petruzzo P, Margreiter R et al.. The International Registry on Hand and Composite Tissue Transplantation.  Transplantation. 2005;  79 1210-1214
    CrossrefPubMedGoogle Scholar
  • 5 Dubernard J M. Composite tissue allografts: a challenge for transplantologists.  Am J Transplant. 2005;  5 1580-1581
    CrossrefPubMedGoogle Scholar
  • 6 Jiang H Q, Wang Y, Hu X B, Li Y S, Li J S. Composite tissue allograft transplantation of cephalocervical skin flap and two ears.  Plast Reconstr Surg. 2005;  115 31e-35e
    CrossrefPubMedGoogle Scholar
  • 7 Hricik D E. Withdrawal of immunosuppression: implications for composite tissue allograft transplantation.  Transplant Proc. 1998;  30 2721-2723
    CrossrefPubMedGoogle Scholar
  • 8 Mackinnon S E, Doolabh V B, Novak C B, Trulock E P. Clinical outcome following nerve allograft transplantation.  Plast Reconstr Surg. 2001;  107 1419-1429
    CrossrefPubMedGoogle Scholar
  • 9 Mackinnon S E, Dellon A L. Anatomy and Physiology of the Peripheral Nerve. Surgery of the Peripheral Nerve. New York, NY; Thieme Medical Publishers 1988: 1-33
    Google Scholar
  • 10 Mackinnon S E, Hudson A R, Hunter D A. Histologic assessment of nerve regeneration in the rat.  Plast Reconstr Surg. 1985;  75 384-388
    PubMedGoogle Scholar
  • 11 Evans G R. Approaches to tissue engineered peripheral nerve.  Clin Plast Surg. 2003;  30 559-563 , viii
    CrossrefPubMedGoogle Scholar
  • 12 Weber R V, Mackinnon S E. Bridging the neural gap.  Clin Plast Surg. 2005;  32 605-616 , viii
    CrossrefPubMedGoogle Scholar
  • 13 Mackinnon S E, Dellon A L. Nerve Repair and Nerve Grafting. Surgery of the Peripheral Nerve. New York, NY; Thieme Medical Publishers 1998: 89-129
    Google Scholar
  • 14 Schlosshauer B, Dreesmann L, Schaller H E, Sinis N. Synthetic nerve guide implants in humans: a comprehensive survey.  Neurosurgery. 2006;  59 740-747
    CrossrefPubMedGoogle Scholar
  • 15 Hadlock T A, Sundback C A, Hunter D A, Vacanti J P, Cheney M L. A new artificial nerve graft containing rolled Schwann cell monolayers.  Microsurgery. 2001;  21 96-101
    CrossrefPubMedGoogle Scholar
  • 16 Rochkind S, Astachov L, el Ani D et al.. Further development of reconstructive and cell tissue-engineering technology for treatment of complete peripheral nerve injury in rats.  Neurol Res. 2004;  26 161-166
    CrossrefPubMedGoogle Scholar
  • 17 Komiyama T, Nakao Y, Toyama Y, Vacanti C A, Vacanti M P, Ignotz R A. Novel technique for peripheral nerve reconstruction in the absence of an artificial conduit.  J Neurosci Methods. 2004;  134 133-140
    CrossrefPubMedGoogle Scholar
  • 18 Mosahebi A, Wiberg M, Terenghi G. Addition of fibronectin to alginate matrix improves peripheral nerve regeneration in tissue-engineered conduits.  Tissue Eng. 2003;  9 209-218
    CrossrefPubMedGoogle Scholar
  • 19 Hou S Y, Zhang H Y, Quan D P, Liu X L, Zhu J K. Tissue-engineered peripheral nerve grafting by differentiated bone marrow stromal cells.  Neuroscience. 2006;  140 101-110
    CrossrefPubMedGoogle Scholar
  • 20 Bryan D J, Holway A H, Wang K K et al.. Influence of glial growth factor and Schwann cells in a bioresorbable guidance channel on peripheral nerve regeneration.  Tissue Eng. 2000;  6 129-138
    CrossrefPubMedGoogle Scholar
  • 21 Xu X, Yee W C, Hwang P Y et al.. Peripheral nerve regeneration with sustained release of poly (phosphoester) microencapsulated nerve growth factor within nerve guide conduits.  Biomaterials. 2003;  24 2405-2412
    CrossrefPubMedGoogle Scholar
  • 22 Myckatyn T M, Mackinnon S E. Surgical techniques of nerve grafting (standard/vascularized/allograft).  Operative Techniques in Orthopedics. 2004;  14 171-178
    PubMedGoogle Scholar
  • 23 Hiles R W. Freeze dried irradiated nerve homograft: a preliminary report.  Hand. 1972;  4 79-84
    CrossrefPubMedGoogle Scholar
  • 24 Gye R S, Hargrave J C, Lowenthal J, Mcleod J G, Pollard J D, Booth G O. Use of immunosuppressive agents in human nerve grafting.  Lancet. 1972;  1 647-650
    PubMedGoogle Scholar
  • 25 Mackinnon S E, Hudson A R. Clinical application of peripheral nerve transplantation.  Plast Reconstr Surg. 1992;  90 695-699
    PubMedGoogle Scholar
  • 26 Gruber S A, Mancias P, Swinford R D, Prashner H R, Clifton J, Henry M H. Living-donor nerve transplantation for global obstetric brachial plexus palsy.  J Reconstr Microsurg. 2006;  22 245-254
    Article in Thieme ConnectPubMedGoogle Scholar
  • 27 Elkwood A I, Kaufman M R, Rose M I et al.. Nerve allograft transplantation for functional restoration of the upper extremity.  Plast Reconstr Surg. 2006;  118(4 Suppl) 9-15
    PubMedGoogle Scholar
  • 28 Mackinnon S E. Nerve allotransplantation following severe tibial nerve injury. Case report.  J Neurosurg. 1996;  84 671-676
    PubMedGoogle Scholar
  • 29 Mackinnon S E, Doolabh V B, Novak C B, Trulock E P. Clinical outcome following nerve allograft transplantation.  Plast Reconstr Surg. 2001;  107 1419-1429
    CrossrefPubMedGoogle Scholar
  • 30 Whitley D, Kupiec-Weglinski W, Tilney N L. Antibody-mediated rejection of organ grafts.  Curr Opin Immunol. 1989;  2 864-869
    PubMedGoogle Scholar
  • 31 Pattison J M, Krensky A M. New insights into mechanisms of allograft rejection.  Am J Med Sci. 1997;  313 257-263
    CrossrefPubMedGoogle Scholar
  • 32 VanBuskirk A M, Pidwell D J, Adams P W, Orosz C G. Transplantation immunology.  JAMA. 1997;  278 1993-1999
    CrossrefPubMedGoogle Scholar
  • 33 Mackinnon S, Hudson A, Falk R, Bilbao J, Kline D, Hunter D. Nerve allograft response: a quantitative immunological study.  Neurosurgery. 1982;  10 61-69
    CrossrefPubMedGoogle Scholar
  • 34 Trumble T, Gunlikson R, Parvin D. A comparison of immune response to nerve and skin allografts.  J Reconstr Microsurg. 1993;  9 367-372
    PubMedGoogle Scholar
  • 35 Ishida O, Ochi M, Ikuta Y, Akiyama M. Peripheral nerve allograft: cellular and humoral immune responses of mice.  J Surg Res. 1990;  49 233-238
    CrossrefPubMedGoogle Scholar
  • 36 Zalewski A A, Silvers W K. An evaluation of nerve repair with nerve allografts in normal and immunologically tolerant rats.  J Neurosurg. 1980;  52 557-563
    CrossrefPubMedGoogle Scholar
  • 37 Pollard J D, Gye R S, McLeod J G. An assessment of immunosuppressive agents in experimental peripheral nerve transplantation.  Surg Gynecol Obstet. 1971;  132 839-845
    PubMedGoogle Scholar
  • 38 Trumble T E, Shon F G. The physiology of nerve transplantation.  Hand Clin. 2000;  16 105-122
    PubMedGoogle Scholar
  • 39 Yu L T, Hickey W F, Silvers W S, LaRossa D, Rostami A M. Expression of class II antigens on peripheral nerve allografts.  Ann N Y Acad Sci. 1988;  540 472-474
    CrossrefPubMedGoogle Scholar
  • 40 Lassner F, Schaller E, Steinhoff G, Wonigeit K, Walter G F, Berger A. Cellular mechanisms of rejection and regeneration in peripheral nerve allografts.  Transplantation. 1989;  48 386-392
    CrossrefPubMedGoogle Scholar
  • 41 Gulati A K. Immune response and neurotrophic factor interactions in peripheral nerve transplants.  Acta Haematol. 1998;  99 171-174
    CrossrefPubMedGoogle Scholar
  • 42 Ansselin A D, Pollard J D. Immunopathological factors in peripheral nerve allograft rejection: quantification of lymphocyte invasion and major histocompatibility complex expression.  J Neurol Sci. 1990;  96 75-88
    CrossrefPubMedGoogle Scholar
  • 43 Ogleznev KIa, Khalikov V A. The validation of the microsurgical plastic repair of damaged peripheral nerves by using allografts (experimental and clinical research).  , [in Russian] Zh Vopr Neirokhir Im N N Burdenko. 1990;  6 8-10
    PubMedGoogle Scholar
  • 44 Mackinnon S E, Hudson A R. Clinical application of peripheral nerve transplantation.  Plast Reconstr Surg. 1992;  90 695-699
    PubMedGoogle Scholar
  • 45 Mackinnon S E. Nerve allotransplantation following severe tibial nerve injury. Case report.  J Neurosurg. 1996;  84 671-676
    PubMedGoogle Scholar
  • 46 Mackinnon S E, Doolabh V B, Novak C B, Trulock E P. Clinical outcome following nerve allograft transplantation.  Plast Reconstr Surg. 2001;  107 1419-1429
    CrossrefPubMedGoogle Scholar
  • 47 Gruber S A, Mancias P, Swinford R D, Prashner H R, Clifton J, Henry M H. Living-donor nerve transplantation for global obstetric brachial plexus palsy.  J Reconstr Microsurg. 2006;  22 245-254
    Article in Thieme ConnectPubMedGoogle Scholar
  • 48 Mackinnon S E. Nerve allotransplantation following severe tibial nerve injury. Case report.  J Neurosurg. 1996;  84 671-676
    PubMedGoogle Scholar
  • 49 Mackinnon S E, Doolabh V B, Novak C B, Trulock E P. Clinical outcome following nerve allograft transplantation.  Plast Reconstr Surg. 2001;  107 1419-1429
    CrossrefPubMedGoogle Scholar
  • 50 Zalewski A A, Fahy G M, Azzam N A, Azzam R N. The fate of cryopreserved nerve isografts and allografts in normal and immunosuppressed rats.  J Comp Neurol. 1993;  331 134-147
    PubMedGoogle Scholar
  • 51 Fansa H, Lassner F, Kook P H, Keilhoff G, Schneider W. Cryopreservation of peripheral nerve grafts.  Muscle Nerve. 2000;  23 1227-1233
    PubMedGoogle Scholar
  • 52 Evans P J, Mackinnon S E, Best T J et al.. Regeneration across preserved peripheral nerve grafts.  Muscle Nerve. 1995;  18 1128-1138
    CrossrefPubMedGoogle Scholar
  • 53 Levi A D, Evans P J, Mackinnon S E, Bunge R P. Cold storage of peripheral nerves: an in vitro assay of cell viability and function.  Glia. 1994;  10 121-131
    CrossrefPubMedGoogle Scholar
  • 54 Evans P J, Mackinnon S E, Levi A D et al.. Cold preserved nerve allografts: changes in basement membrane, viability, immunogenicity, and regeneration.  Muscle Nerve. 1998;  21 1507-1522
    CrossrefPubMedGoogle Scholar
  • 55 Hare G M, Evans P J, Mackinnon S E et al.. Effect of cold preservation on lymphocyte migration into peripheral nerve allografts in sheep.  Transplantation. 1993;  56 154-162
    PubMedGoogle Scholar
  • 56 Hare G M, Evans P J, Mackinnon S E, Wade J A, Young A J, Hay J B. Phenotypic analysis of migrant, efferent lymphocytes after implantation of cold preserved, peripheral nerve allografts.  J Neuroimmunol. 1995;  56 9-16
    PubMedGoogle Scholar
  • 57 Strasberg S R, Mackinnon S E, Hare G M, Narini P P, Hertl C, Hay J B. Reduction in peripheral nerve allograft antigenicity with warm and cold temperature preservation.  Plast Reconstr Surg. 1996;  97 152-160
    PubMedGoogle Scholar
  • 58 Atchabahian A, Mackinnon S E, Hunter D A. Cold preservation of nerve grafts decreases expression of ICAM-1 and class II MHC antigens.  J Reconstr Microsurg. 1999;  15 307-311
    Article in Thieme ConnectPubMedGoogle Scholar
  • 59 Fox I K, Jaramillo A, Hunter D A, Rickman S R, Mohanakumar T, Mackinnon S E. Prolonged cold preservation of nerve allografts yields a non-immunogenic graft. 2004
    Google Scholar
  • 60 Mackinnon S E, Hudson A R, Falk R E, Kline D, Hunter D. Peripheral nerve allograft: an assessment of regeneration across pretreated nerve allografts.  Neurosurgery. 1984;  15 690-693
    PubMedGoogle Scholar
  • 61 Dumont C E, Hentz V R. Enhancement of axon growth by detergent-extracted nerve grafts.  Transplantation. 1997;  63 1210-1215
    PubMedGoogle Scholar
  • 62 Mligiliche N, Tabata Y, Endoh K, Ide C. Peripheral nerve regeneration through a long detergent-denatured muscle autografts in rabbits.  Neuroreport. 2001;  12 1719-1722
    PubMedGoogle Scholar
  • 63 Haase S C, Rovak J M, Dennis R G, Kuzon Jr W M, Cederna P S. Recovery of muscle contractile function following nerve gap repair with chemically acellularized peripheral nerve grafts.  J Reconstr Microsurg. 2003;  19 241-248
    Article in Thieme ConnectPubMedGoogle Scholar
  • 64 Fansa H, Keilhoff G, Wolf G, Schneider W. Tissue engineering of peripheral nerves: A comparison of venous and acellular muscle grafts with cultured Schwann cells.  Plast Reconstr Surg. 2001;  107 485-494
    PubMedGoogle Scholar
  • 65 Frerichs O, Fansa H, Schicht C, Wolf G, Schneider W, Keilhoff G. Reconstruction of peripheral nerves using acellular nerve grafts with implanted cultured Schwann cells.  Microsurgery. 2002;  22 311-315
    CrossrefPubMedGoogle Scholar
  • 66 Brenner M J, Lowe J BI, Fox I K et al.. Effects of Schwann cells and donor antigen on long nerve allograft regeneration.  Microsurgery. , (in press)
    PubMedGoogle Scholar
  • 67 Hess J R, Brenner M J, Fox I K et al.. Use of cold-preserved allografts seeded with autlogous Schwann cells in the treatment of a long-gap peripheral nerve injury.  Plast Reconstr Surg. 2007;  119 246-259
    CrossrefPubMedGoogle Scholar
  • 68 Levi A D, Guenard V, Aebischer P, Bunge R P. The functional characteristics of Schwann cells cultured from human peripheral nerve after transplantation into a gap within the rat sciatic nerve.  J Neurosci. 1994;  14(3 Pt 1) 1309-1319
    PubMedGoogle Scholar
  • 69 Hattori Y, Doi K, Ikeda K, Pagsaligan J M. Vascularized ulnar nerve graft for reconstruction of a large defect of the median or radial nerves after severe trauma of the upper extremity.  J Hand Surg [Am]. 2005;  30 986-989
    PubMedGoogle Scholar
  • 70 Koshima I, Murashita T, Soeda S. Free vascularized deep peroneal neurocutaneous flap for repair of digital nerve defect involving severe finger damage.  J Hand Surg [Am]. 1991;  16 227-229
    CrossrefPubMedGoogle Scholar
  • 71 Koshima I, Nanba Y, Tsutsui T, Takahashi Y, Kawai A. Vascularized femoral nerve graft with anterolateral thigh true perforator flap for massive defects after cancer ablation in the upper arm.  J Reconstr Microsurg. 2003;  19 299-302
    Article in Thieme ConnectPubMedGoogle Scholar
  • 72 Sen S K, Lowe III J B, Brenner M J, Hunter D A, Mackinnon S E. Assessment of the immune response to dose of nerve allografts.  Plast Reconstr Surg. 2005;  115 823-830
    CrossrefPubMedGoogle Scholar
  • 73 Best T J, Mackinnon S E, Midha R, Hunter D A, Evans P J. Revascularization of peripheral nerve autografts and allografts.  Plast Reconstr Surg. 1999;  104 152-160
    CrossrefPubMedGoogle Scholar
  • 74 Best T J, Mackinnon S E, Evans P J, Hunter D, Midha R. Peripheral nerve revascularization: histomorphometric study of small- and large-caliber grafts.  J Reconstr Microsurg. 1999;  15 183-190
    PubMedGoogle Scholar
  • 75 Myckatyn T M, Mackinnon S E. Surgical Techniques of Nerve Grafting (Standard/Vascularized/Allograft). 14, 171-177 2004
    Google Scholar
  • 76 Mackinnon S E, Doolabh V B, Novak C B, Trulock E P. Clinical outcome following nerve allograft transplantation.  Plast Reconstr Surg. 2001;  107 1419-1429
    CrossrefPubMedGoogle Scholar
  • 77 Lyons W E, George E B, Dawson T M, Steiner J P, Snyder S H. Immunosuppressant FK506 promotes neurite outgrowth in cultures of PC12 cells and sensory ganglia.  Proc Natl Acad Sci U S A. 1994;  91 3191-3195
    CrossrefPubMedGoogle Scholar
  • 78 Steiner J P, Connolly M A, Valentine H L et al.. Neurotrophic actions of nonimmunosuppressive analogues of immunosuppressive drugs FK506, rapamycin and cyclosporin A.  Nat Med. 1997;  3 421-428
    CrossrefPubMedGoogle Scholar
  • 79 Chunasuwankul R, Ayrout C, Dereli Z, Gal A, Lanzetta M, Owen E. Low dose discontinued FK506 treatment enhances peripheral nerve regeneration.  Int Surg. 2002;  87 274-278
    PubMedGoogle Scholar
  • 80 Doolabh V B, Mackinnon S E. FK506 accelerates functional recovery following nerve grafting in a rat model.  Plast Reconstr Surg. 1999;  103 1928-1936
    CrossrefPubMedGoogle Scholar
  • 81 Fansa H, Keilhoff G, Altmann S, Plogmeier K, Wolf G, Schneider W. The effect of the immunosuppressant FK 506 on peripheral nerve regeneration following nerve grafting.  J Hand Surg [Br]. 1999;  24 38-42
    CrossrefPubMedGoogle Scholar
  • 82 Gold B G, Storm-Dickerson T, Austin D R. The immunosuppressant FK506 increases functional recovery and nerve regeneration following peripheral nerve injury.  Restor Neurol Neurosci. 1994;  6 287-296
    PubMedGoogle Scholar
  • 83 Gold B G, Gordon H S, Wang M S. Efficacy of delayed or discontinuous FK506 administrations on nerve regeneration in the rat sciatic nerve crush model: lack of evidence for a conditioning lesion-like effect.  Neurosci Lett. 1999;  267 33-36
    CrossrefPubMedGoogle Scholar
  • 84 Jost S C, Doolabh V B, Mackinnon S E, Lee M, Hunter D A. Acceleration of peripheral nerve regeneration following FK506 administration.  Restor Neurol Neurosci. 2000;  17 39-44
    PubMedGoogle Scholar
  • 85 Lee M, Doolabh V B, Mackinnon S E, Jost S. FK506 promotes functional recovery in crushed rat sciatic nerve.  Muscle Nerve. 2000;  23 633-640
    CrossrefPubMedGoogle Scholar
  • 86 Wang M S, Zeleny-Pooley M, Gold B G. Comparative dose-dependence study of FK506 and cyclosporin A on the rate of axonal regeneration in the rat sciatic nerve.  J Pharmacol Exp Ther. 1997;  282 1084-1093
    PubMedGoogle Scholar
  • 87 Yang R K, Lowe III J B, Sobol J B, Hunter D A, Mackinnon S E. Dose-dependent effects of FK506 on neuroregeneration in a rat model.  Plast Reconstr Surg. 2003; 
    PubMedGoogle Scholar
  • 88 Udina E, Ceballos D, Verdu E, Gold B G, Navarro X. Bimodal dose-dependence of FK506 on the rate of axonal regeneration in mouse peripheral nerve.  Muscle Nerve. 2002;  26 348-355
    CrossrefPubMedGoogle Scholar
  • 89 Udina E, Ceballos D, Gold B G et al.. FK-506 enhances reinnervation by regeneration and by collateral sprouting of peripheral nerve fibers.  Exp Neurol. 2003;  183 220-231
    CrossrefPubMedGoogle Scholar
  • 90 Gold B G, Densmore V, Shou W, Matzuk M M, Gordon H S. Immunophilin FK506-binding protein 52 (not FK506-binding protein 12) mediates the neurotrophic action of FK506.  J Pharmacol Exp Ther. 1999;  289 1202-1210
    PubMedGoogle Scholar
  • 91 Katsube K, Doi K, Fukumoto T, Fujikura Y, Shigetomi M, Kawai S. Nerve regeneration and origin of Schwann cells in peripheral nerve allografts in immunologically pretreated rats.  Transplantation. 1996;  62 1643-1649
    CrossrefPubMedGoogle Scholar
  • 92 Brenner M J, Tung T H, Mackinnon S E, Myckatyn T M, Hunter D A, Mohanakumar T. Anti-CD40 ligand monoclonal antibody induces a permissive state, but not tolerance, for murine peripheral nerve allografts.  Exp Neurol. 2004;  186 59-69
    CrossrefPubMedGoogle Scholar
  • 93 Brenner M J, Jensen J N, Lowe III J B et al.. Anti-CD40 ligand antibody permits regeneration through peripheral nerve allografts in a nonhuman primate model.  Plast Reconstr Surg. 2004;  114 1802-1814
    CrossrefPubMedGoogle Scholar
  • 94 Scharpf J, Strome M, Siemionow M. Immunomodulation with anti-alphabeta T-cell receptor monoclonal antibodies in combination with cyclosporine A improves regeneration in nerve allografts.  Microsurgery. 2006; 
    PubMedGoogle Scholar
  • 95 Brenner M J, Lowe III J B, Fox I K et al.. Effects of Schwann cells and donor antigen on long-nerve allograft regeneration.  Microsurgery. 2005;  25 61-70
    CrossrefPubMedGoogle Scholar
  • 96 Genden E M, Mackinnon S E, Yu S, Hunter D A, Flye M W. Pretreatment with portal venous ultraviolet B-irradiated donor alloantigen promotes donor-specific tolerance to rat nerve allografts.  Laryngoscope. 2001;  111 439-447
    PubMedGoogle Scholar
  • 97 Genden E M, Mackinnon S E, Yu S, Flye M W. Induction of donor-specific tolerance to rat nerve allografts with portal venous donor alloantigen and anti-ICAM-1/LFA-1 monoclonal antibodies.  Surgery. 1998;  124 448-456
    CrossrefPubMedGoogle Scholar
  • 98 Brushart T M, Seiler W A. Selective reinnervation of distal motor stumps by peripheral motor axons.  Exp Neurol. 1987;  97 289-300
    CrossrefPubMedGoogle Scholar
  • 99 Brushart T M. Preferential reinnervation of motor nerves by regenerating motor axons.  J Neurosci. 1988;  8 1026-1031
    PubMedGoogle Scholar
  • 100 Brushart T M. Motor axons preferentially reinnervate motor pathways.  J Neurosci. 1993;  13 2730-2738
    Google Scholar
  • 101 Brenner M J, Hess J R, Myckatyn T M, Hayashi A, Hunter D A, Mackinnon S E. Repair of motor nerve gaps with sensory nerve inhibits regeneration in rats.  Laryngoscope. 2006;  116 1685-1692
    CrossrefPubMedGoogle Scholar
  • 102 Nichols C M, Brenner M J, Fox I K et al.. Effects of motor versus sensory nerve grafts on peripheral nerve regeneration.  Exp Neurol. 2004;  190 347-355
    CrossrefPubMedGoogle Scholar

Susan E MackinnonM.D. 

Shoenberg Professor and Chair, Division of Plastic Surgery, Washington University School of Medicine, Box 8238

660 S. Euclid Avenue, Saint Louis, MO 63110